Transcranial magnetic stimulation facilitates neurorehabilitation after pediatric traumatic brain injury

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Lu, Hongyang ^a,b,c   Kobilo, Tali ^a,b   Robertson, Courtney ^b   Tong, Shanbao ^c   Celnik, Pablo ^b   Pelled, Galit ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CN17BETA PEPTIDE; PEPTIDE FRAGMENT;

ANIMAL; BRAIN CORTEX; BRAIN INJURIES, TRAUMATIC; DISEASE MODEL; HUMAN; MALE; METABOLISM; NERVE CELL PLASTICITY; NEUROREHABILITATION; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; TRANSCRANIAL MAGNETIC STIMULATION;

ANIMALS; BRAIN INJURIES, TRAUMATIC; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROLOGICAL REHABILITATION; NEURONAL PLASTICITY; PEPTIDE FRAGMENTS; RATS, SPRAGUE-DAWLEY; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84943228294     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep14769     Document Type: Article

References (73)

1. Xiong, Y., Mahmood, A., Chopp, M. Animal models of traumatic brain injury. Nat Rev Neurosci 14, 128-142 (2013).
2. Walker, P. A. et al. Modern approaches to pediatric brain injury therapy. J Trauma 67, S120-127 (2009).
3. Popernack, M. L., Gray, N., Reuter-Rice, K. Moderate-to-Severe Traumatic Brain Injury in Children: Complications and Rehabilitation Strategies. J Pediatr Health Care 29, e1-e7 (2014).
4. Cantore, L., Norwood, K., Patrick, P. Medical aspects of pediatric rehabilitation after moderate to severe traumatic brain injury. NeuroRehabilitation 30, 225-234 (2012).
5. Barlow, K. M., Thomson, E., Johnson, D., Minns, R. A. Late neurologic and cognitive sequelae of inflicted traumatic brain injury in infancy. Pediatrics 116, e174-185 (2005).
6. Yeates, K. O. et al. Short-and long-term social outcomes following pediatric traumatic brain injury. J Int Neuropsychol Soc 10, 412-426 (2004).
7. Wechsler, B., Kim, H., Gallagher, P. R., DiScala, C., Stineman, M. G. Functional status after childhood traumatic brain injury. J Trauma 58, 940-949 (2005).
8. Rosema, S. et al. The trajectory of long-term psychosocial development 16 years following childhood traumatic brain injury. J Neurotrauma 32, 976-983 (2015).
9. Wilde, E. A. et al. Diffusion tensor imaging in the corpus callosum in children after moderate to severe traumatic brain injury. J Neurotrauma 23, 1412-1426 (2006).
10. Ewing-Cobbs, L. et al. Arrested development and disrupted callosal microstructure following pediatric traumatic brain injury: relation to neurobehavioral outcomes. Neuroimage 42, 1305-1315 (2008).
11. Li, N. et al. Evidence for impaired plasticity after traumatic brain injury in the developing brain. J Neurotrauma 31, 395-403 (2014).
12. Arango, J. I. et al. Posttraumatic seizures in children with severe traumatic brain injury. Childs Nerv Syst 28, 1925-1929 (2012).
13. Matsumoto, J. H. et al. Prevalence of epileptic and nonepileptic events after pediatric traumatic brain injury. Epilepsy Behav 27, 233-237 (2013).
14. Statler, K. D. et al. A potential model of pediatric posttraumatic epilepsy. Epilepsy Res 86, 221-223 (2009).
15. Ip, E. Y., Giza, C. C., Griesbach, G. S., Hovda, D. A. Effects of enriched environment and fluid percussion injury on dendritic arborization within the cerebral cortex of the developing rat. J Neurotrauma 19, 573-585 (2002).
16. D'Ambrosio, R., Maris, D. O., Grady, M. S., Winn, H. R., Janigro, D. Selective loss of hippocampal long-term potentiation, but not depression, following fluid percussion injury. Brain Res 786, 64-79 (1998).
17. Prince, D. A., Tseng, G. F. Epileptogenesis in chronically injured cortex: in vitro studies. J Neurophysiol 69, 1276-1291 (1993).
18. Ping, X., Jin, X. Transition from initial hypoactivity to hyperactivity in cortical layer V pyramidal neurons following traumatic brain injury in vivo. J Neurotrauma (2015).
19. Johnstone, V. P., Shultz, S. R., Yan, E. B., O'Brien, T. J., Rajan, R. The acute phase of mild traumatic brain injury is characterized by a distance-dependent neuronal hypoactivity. J Neurotrauma 31, 1881-1895 (2014).
20. Johnston, M. V. Plasticity in the developing brain: implications for rehabilitation. Dev Disabil Res Rev 15, 94-101 (2009).
21. Schulz, R., Gerloff, C., Hummel, F. C. Non-invasive brain stimulation in neurological diseases. Neuropharmacology 64, 579-587 (2013).
22. Celnik, P. A., Cohen, L. G. Modulation of motor function and cortical plasticity in health and disease. Restor Neurol Neurosci 22, 261-268 (2004).
23. Lefaucheur, J. P. et al. Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J Neurol Neurosurg Psychiatry 75, 612-616 (2004).
24. Nardone, R. et al. Invasive and non-invasive brain stimulation for treatment of neuropathic pain in patients with spinal cord injury: a review. J Spinal Cord Med 37, 19-31 (2013).
25. Leo, R. J., Latif, T. Repetitive transcranial magnetic stimulation (rTMS) in experimentally induced and chronic neuropathic pain: a review. J Pain 8, 453-459 (2007).
26. Demirtas-Tatlidede, A., Vahabzadeh-Hagh, A. M., Bernabeu, M., Tormos, J. M., Pascual-Leone, A. Noninvasive brain stimulation in traumatic brain injury. J Head Trauma Rehabil 27, 274-292 (2012).
27. Villamar, M. F., Santos Portilla, A., Fregni, F., Zafonte, R. Noninvasive brain stimulation to modulate neuroplasticity in traumatic brain injury. Neuromodulation 15, 326-338 (2012).
28. Pape, T. L., Rosenow, J., Lewis, G. Transcranial magnetic stimulation: a possible treatment for TBI. J Head Trauma Rehabil 21, 437-451 (2006).
29. Adelson, P. D., Whalen, M. J., Kochanek, P. M., Robichaud, P., Carlos, T. M. Blood brain barrier permeability and acute inflammation in two models of traumatic brain injury in the immature rat: a preliminary report. Acta Neurochir Suppl 71, 104-106 (1998).
30. Pullela, R. et al. Traumatic injury to the immature brain results in progressive neuronal loss, hyperactivity and delayed cognitive impairments. Dev Neurosci 28, 396-409 (2006).
31. Scafidi, S., Racz, J., Hazelton, J., McKenna, M. C., Fiskum, G. Neuroprotection by acetyl-L-carnitine after traumatic injury to the immature rat brain. Dev Neurosci 32, 480-487 (2010).
32. Robertson, C. L., Saraswati, M., Fiskum, G. Mitochondrial dysfunction early after traumatic brain injury in immature rats. J Neurochem 101, 1248-1257 (2007).
33. Prins, M. L., Povlishock, J. T., Phillips, L. L. The effects of combined fluid percussion traumatic brain injury and unilateral entorhinal deafferentation on the juvenile rat brain. Brain Res Dev Brain Res 140, 93-104 (2003).
34. Siebner, H. R., Rothwell, J. Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148, 1-16 (2003).
35. Cowen, T. D. et al. Influence of early variables in traumatic brain injury on functional independence measure scores and rehabilitation length of stay and charges. Arch Phys Med Rehabil 76, 797-803 (1995).
36. Adelson, P. D., Dixon, C. E., Kochanek, P. M. Long-term dysfunction following diffuse traumatic brain injury in the immature rat. J Neurotrauma 17, 273-282 (2000).
37. Scheibel, R. S. et al. Altered brain activation during cognitive control in patients with moderate to severe traumatic brain injury. Neurorehabil Neural Repair 21, 36-45 (2007).
38. Christodoulou, C. et al. Functional magnetic resonance imaging of working memory impairment after traumatic brain injury. J Neurol Neurosurg Psychiatry 71, 161-168 (2001).
39. Chen, J. K. et al. Functional abnormalities in symptomatic concussed athletes: an fMRI study. Neuroimage 22, 68-82 (2004).
40. Lovell, M. R. et al. Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery 61, 352-359 (2007).
41. Newsome, M. R. et al. Brain activation during working memory after traumatic brain injury in children. Neurocase 13, 16-24 (2007).
42. Niskanen, J. P. et al. Monitoring functional impairment and recovery after traumatic brain injury in rats by FMRI. J Neurotrauma 30, 546-556 (2013).
43. Mishra, A. M. et al. Decreased resting functional connectivity after traumatic brain injury in the rat. PLoS One 9, e95280 (2014).
44. Max, J. E. et al. Anxiety disorders in children and adolescents in the first six months after traumatic brain injury. J Neuropsychiatry Clin Neurosci 23, 29-39 (2011).
45. Li, L., Liu, J. The effect of pediatric traumatic brain injury on behavioral outcomes: a systematic review. Dev Med Child Neurol 55, 37-45 (2013).
46. Ajao, D. O. et al. Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood. J Neurotrauma 29, 2060-2074 (2012).
47. Semple, B. D., Canchola, S. A., Noble-Haeusslein, L. J. Deficits in social behavior emerge during development after pediatric traumatic brain injury in mice. J Neurotrauma 29, 2672-2683 (2012).
48. Bloom, D. R. et al. Lifetime and novel psychiatric disorders after pediatric traumatic brain injury. J Am Acad Child Adolesc Psychiatry 40, 572-579 (2001).
49. Konrad, K., Gauggel, S., Manz, A., Scholl, M. Inhibitory control in children with traumatic brain injury (TBI) and children with attention deficit/hyperactivity disorder (ADHD). Brain Inj 14, 859-875 (2000).
50. Giza, C. C., Prins, M. L. Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury. Dev Neurosci 28, 364-379 (2006).
51. Koski, L. et al. Noninvasive brain stimulation for persistent postconcussion symptoms in mild traumatic brain injury. J Neurotrauma 32, 38-44 (2015).
52. Frye, R. E., Rotenberg, A., Ousley, M., Pascual-Leone, A. Transcranial magnetic stimulation in child neurology: current and future directions. J Child Neurol 23, 79-96 (2008).
53. Casanova, M. F. et al. Effects of weekly low-frequency rTMS on autonomic measures in children with autism spectrum disorder. Front Hum Neurosci 8, 851 (2014).
54. Quintana, H. Transcranial magnetic stimulation in persons younger than the age of 18. J ECT 21, 88-95 (2005).
55. Wassermann, E. M. et al. Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 101, 412-417 (1996).
56. Chen, R. et al. Safety of different inter-train intervals for repetitive transcranial magnetic stimulation and recommendations for safe ranges of stimulation parameters. Electroencephalogr Clin Neurophysiol 105, 415-421 (1997).
57. Pascual-Leone, A. et al. Safety of rapid-rate transcranial magnetic stimulation in normal volunteers. Electroencephalogr Clin Neurophysiol 89, 120-130 (1993).
58. Garvey, M. A., Gilbert, D. L. Transcranial magnetic stimulation in children. Eur J Paediatr Neurol 8, 7-19 (2004).
59. Rossi, S., Hallett, M., Rossini, P. M., Pascual-Leone, A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 120, 2008-2039 (2009).
60. Mueller, J. K. et al. Simultaneous transcranial magnetic stimulation and single-neuron recording in alert non-human primates. Nat Neurosci 17, 1130-1136 (2014).
61. Pashut, T. et al. Patch-clamp recordings of rat neurons from acute brain slices of the somatosensory cortex during magnetic stimulation. Front Cell Neurosci 8, 145 (2014).
62. Pascual-Leone, A., Valls-Sole, J., Wassermann, E. M., Hallett, M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117 (Pt 4), 847-858 (1994).
63. Benali, A. et al. Theta-burst transcranial magnetic stimulation alters cortical inhibition. J Neurosci 31, 1193-1203 (2011).
64. Vlachos, A. et al. Repetitive magnetic stimulation induces functional and structural plasticity of excitatory postsynapses in mouse organotypic hippocampal slice cultures. J Neurosci 32, 17514-17523 (2012).
65. Duffau, H. Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J Clin Neurosci 13, 885-897 (2006).
66. Di Battista, A., Godfrey, C., Soo, C., Catroppa, C., Anderson, V. Depression and health related quality of life in adolescent survivors of a traumatic brain injury: a pilot study. PLoS One 9, e101842 (2014).
67. Karver, C. L. et al. Age at injury and long-term behavior problems after traumatic brain injury in young children. Rehabil Psychol 57, 256-265 (2012).
68. Gersner, R., Kravetz, E., Feil, J., Pell, G., Zangen, A. Long-term effects of repetitive transcranial magnetic stimulation on markers for neuroplasticity: differential outcomes in anesthetized and awake animals. J Neurosci 31, 7521-7526 (2011).
69. Yukimasa, T. et al. High-frequency repetitive transcranial magnetic stimulation improves refractory depression by influencing catecholamine and brain-derived neurotrophic factors. Pharmacopsychiatry 39, 52-59 (2006).
70. Li, N., van Zijl, P., Thakor, N., Pelled, G. Study of the Spatial Correlation Between Neuronal Activity and BOLD fMRI Responses Evoked by Sensory and Channelrhodopsin-2 Stimulation in the Rat Somatosensory Cortex. J Mol Neurosci 53, 553-561 (2014).
71. Pawela, C. P. et al. Resting-state functional connectivity of the rat brain. Magn Reson Med 59, 1021-1029 (2008).
72. Smith, S. M. et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1, S208-219 (2004).
73. Fujimoto, S. T. et al. Motor and cognitive function evaluation following experimental traumatic brain injury. Neurosci Biobehav Rev 28, 365-378 (2004).